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DOI: 10.1002/anie.201311136
Organic–Inorganic Hybrid Materials Hot Paper
Engineering Multifunctional Capsules through the Assembly of Metal– Phenolic Networks** Junling Guo, Yuan Ping, Hirotaka Ejima, Karen Alt, Mirko Meissner, Joseph J. Richardson, Yan Yan, Karlheinz Peter, Dominik v. Elverfeldt, Christoph E. Hagemeyer, and Frank Caruso* Abstract: Metal–organic coordination materials are of widespread interest because of the coupled benefits of inorganic and organic building blocks. These materials can be assembled into hollow capsules with a range of properties, which include selective permeability, enhanced mechanical/thermal stability, and stimuli-responsiveness. Previous studies have primarily focused on the assembly aspects of metal-coordination capsules; however, the engineering of metal-specific functionality for capsule design has not been explored. A library of functional metal–phenolic network (MPN) capsules prepared from a phenolic ligand (tannic acid) and a range of metals is reported. The properties of the MPN capsules are determined by the coordinated metals, allowing for control over film thickness, disassembly characteristics, and fluorescence behavior. Furthermore, the functional properties of the MPN capsules were tailored for drug delivery, positron emission tomography (PET), magnetic resonance imaging (MRI), and catalysis. The ability to incorporate multiple metals into MPN capsules demonstrates that a diverse range of functional materials can be generated.
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aturally occurring building blocks that can assemble into functional materials have long been a source for scientific inspiration.[1] A salient feature of natural materials is the exploitation of organic and inorganic building blocks to prepare hybrid materials with synergistic properties to meet complex biological requirements.[1a,d] For example, by using mild conditions to generate highly functional macroscopic inorganic–organic hybrids, crustaceans produce armoured carapaces,[1d] mollusks build ornate shells,[2] and vertebrates grow lightweight bones.[1d] Specifically, the coordination of
[*] J. Guo, Dr. Y. Ping, Dr. H. Ejima, J. J. Richardson, Dr. Y. Yan, Prof. F. Caruso Department of Chemical and Biomolecular Engineering The University of Melbourne, Parkville Victoria 3010 (Australia) E-mail: [email protected] Dr. K. Alt, Prof. K. Peter, Assoc. Prof. C. E. Hagemeyer Atherothrombosis and Vascular Biology/Vascular Biotechnology Baker IDI Heart and Diabetes Institute Melbourne, Victoria 3010 (Australia) M. Meissner, Prof. D. v. . Elverfeldt Department of Radiology, Medical Physics University Medical Center Freiburg Breisacher Str. 60a, Freiburg (Germany) [**] The authors acknowledge support of this research by the Australian Research Council under the Australian Laureate Fellowship FL120100030 (F.C.), Discovery Project DP0877360 (F.C.), Discovery Early Career Researcher Award DE130100488 (Y.Y.), and Future
Fellowship FT0992210 (K.P.) schemes. This work was supported by a project grant from the National Health and Medical Research Council (grant number 1029249; K.P. and C.E.H.). K.A. is supported by the German Research Foundation (grant number Al 1521/1-1). C.E.H. is supported by a National Heart Foundation Career Development Fellowship (grant number CR 11M 6066). The work was also supported in part by the Victorian Government’s Operational Infrastructure Support Program, Monash Biomedical Imaging and Victoria’s Science Agenda Strategic Project Fund. We acknowledge the Centre for PET at the Austin (Melbourne, Australia) for supply of the 64Cu. We thank X. Wang (Sichuan University) for assistance with the catalytic experiments, X. Duan (The University of Melbourne) for assistance with XPS analysis, Dr. K. Liang (The University of Melbourne) for assistance with deconvolution microscopy, and Dr. Ming Hu, Dr. Jiwei Cui, Yi Ju, and Tomoya Suma (The University of Melbourne) for helpful discussions. Supporting information for this article is available on the WWW under http://dx.doi.org/10.1002/anie.201311136.
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organic ligands with specific metal species plays a critical role in a range of biological functions,[3] such as photosynthesis (through MgII-porphyrin),[4] oxygen transportation (through CuII-heme)[5] and adhesion (through FeIII-phenolics).[6] Inspired by these natural examples, metal–organic coordination materials have attracted considerable interest in chemistry and materials science.[7] The assembly of metal–organic coordination materials into hollow capsules has recently attracted interest because of their desirable properties,[8] such as selective permeability,[9] high mechanical[10] and thermal[11] stability, and pH-responsive disassembly.[10b] Several assembly techniques, including liquid–liquid interfacial growth,[9a] spray-drying,[9b] and sacrificial template-mediated formation,[10–12] have been used to fabricate capsules based on metal-coordination interactions. However, these previous studies have not focused on the specific incorporation of a range of metals into the capsule shells, nor have the incorporated metals specifically been used to impart functionality into the capsules. The ability to incorporate diverse metals into metal–organic coordination capsules provides new opportunities for engineering multifunctional systems for various applications. Here, we demonstrate that a single organic ligand can coordinate with a variety of metals, and thereby provide a broad library of functional metal–phenolic networks (MPNs). Because of the diverse chelation ability of phenolic materials,[13] tannic acid (TA; see Figure S1 in the Supporting Information), a ubiquitous natural polyphenol, is coordinated to 18 different metal ions (M), including aluminium (Al), vanadium (V), chromium (Cr), manganese (Mn), iron (Fe), cobalt (Co), nickel (Ni), copper (Cu), zinc (Zn), zirconium
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. Angewandte Communications Furthermore, the XPS survey scan spectra confirmed the presence of metal in the capsule shells (Figure S4). TA showed a major peak at 533.5 eV and a relatively small peak at 529.4 eV, which can be ascribed to the C=O and HOC groups, respectively.[14] After chelation with metal ions, the peak of the HOC group in the O1s spectra shifted from 529.4 eV to a higher binding energy of 531.8 eV (Figure S5, CuII-TA capsules), which suggests electron transfer from TA to the metals.[15] The MPN films (CuII-TA) are amorphous materials, as confirmed by X-ray diffraction data (Figure S6).[16] The morphology of the capsules was characterized by differential interference contrast (DIC) microscopy, scanning electron microscopy (SEM), transmission electron microscopy (TEM), and atomic force microscopy (AFM) (Figure 2, Figures S7 and S8). The MPN capsules were monodisperse and spherical, as observed by DIC microscopy and freezedried SEM (Figure 2 a, inset). SEM, TEM, and AFM showed collapsed capsules, with folds and creases similar to air-dried polymeric hollow capsules.[17] No excess coordination cluster aggregates were observed on the surface of the MPN capsules in TEM (Figure 2 b) or AFM (Figure 2 c). Energy-dispersive X-ray (EDX) mapping analysis of MPN capsules Figure 1. Assembly of MPN capsules from various metals. a) Assembly of TA and metal ions to form a MPN demonstrated that the metal film on a particulate template, followed by the subsequent formation of a MPN capsule. b) Periodic table: distribution patterns metals highlighted in orange are used to form MPN capsules in this study. Metals highlighted in green show other metals that may be used for MPN capsule preparation based on previous studies on metal-coordination matched well with highwith phenolics in bulk solution. c) DIC images of MPN capsules prepared from different metals. Scale bars angle annular dark-field are 5 mm. Inset images are photographs of MPN capsule suspensions. images (HAADF) and the distribution patterns of C and O maps (Figure 2 d). This confirms that the metals were associated with TA and MPN films were formed simply by mixing TA and metal well distributed in the MPN films. AFM was used to probe the solutions in the presence of a substrate (Figure 1 a). When material differences between MPN capsules prepared from using particulate templates, highly monodisperse capsules metals of different oxidation numbers: CuII-TA, AlIII-TA, and containing a broad range of metals were obtained after template removal (Figure 1 c). The coordination between TA ZrIV-TA (Figure S9). The thickness and stability of the MPN and metals was confirmed by UV/Vis absorption spectrophofilms are dependent on the choice of metal and the metal feed tometry, Fourier transform infrared spectrophotometry (FTconcentration (hereafter denoted [M]). Notably, comparison IR) and X-ray photoelectron spectroscopy (XPS). UV/Vis of film thicknesses among these three MPN capsules showed spectra of MPN capsule suspensions show new absorbance that ZrIV-TA capsules were the thickest and CuII-TA capsules peaks after metal chelation, which suggests coordination the thinnest. The film thickness of CuII-TA capsules increased between TA and the respective metals (Figure S2). FT-IR from 9.0 0.8 nm to 10.7 1.5 nm when the feed [CuII] III spectra of the Fe -TA MPN capsules (air-dried) also indicate changed from 0.08 ([CuII]:[TA] = 1:3) to 0.72 mm that the phenolic groups coordinated with metal ions, as ([CuII]:[TA] = 3:1). Similarly, the minimum thickness of evidenced by the reduced intensity of the HOC stretching ZrIV-TA capsules was 11.9 1.2 nm ([ZrIV]:[TA] = 1:3), and peak when compared with non-coordinated TA (Figure S3). raising the [ZrIV] increased the film thickness to 15.4 2.2 nm
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(Zr), molybdenum (Mo), ruthenium (Ru), rhodium (Rh), cadmium (Cd), cerium (Ce), europium (Eu), gadolinium (Gd), and terbium (Tb), to generate robust MPN films capable of forming hollow structured capsules (Figure 1). Given the facile preparation process, and the capacity to incorporate single and multiple metals, MPN capsules are a promising class of multifunctional materials. These MPN capsules are herein characterized and used for diverse applications, including drug delivery, biomedical imaging, and catalysis.
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ally disassemble at lower pH values that correspond to those in endosomal and lysosomal compartments (5.0– 6.0). The cytotoxicity of the AlIII-TA capsules was determined to be negligible (Figure S10), hence the drug delivery properties of the AlIII-TA capsules were investigated with model cargo (dextranfluorescein isothiocyanate, FITC-dextran). These capsules were incubated with JAWS II cells for different times. The cellular membranes were stained with AlexaFluor (AF) 594-wheat germ agglutinin, and internalization of Figure 2. Structural characterization of MPN capsules. a) SEM, b) TEM, and c) AFM images of CuII-TA these capsules was verified by capsules. d) EDX elemental mapping of CuII-TA, AlIII-TA and ZrIV-TA capsules. Scale bars are 2 mm in (a–c), deconvolution fluorescence 2 mm in the inset of (a), 200 nm in the inset of (b) and 1 mm in (d). microscopy (Figure 3 b). At the time interval of 16 h, most internalized AlIII-TA IV III capsules were intact, retaining their original spherical shape ([Zr ]:[TA] = 3:1). The film thicknesses of Al -TA films, (see yellow arrows in Figure 3 b). With increasing incubation which increased from 9.9 1.3 nm to 13.6 1.3 nm, showed time (to 24 h), a larger number of deformed and disassembled a similar trend to CuII-TA and ZrIV-TA. We note that below AlIII-TA capsules were observed (see white arrows in Figa [M] of 0.08 mm, capsules for all three metals were difficult to form, while above 0.72 mm the capsules aggregated. ure 3 b). The intracellular disassembly of AlIII-TA capsules The pH-disassembly kinetics of the MPN capsules preprovides the potential for tailored drug release, which is of pared from each of the three model metals (CuII, AlIII, ZrIV) importance for advanced drug delivery.[18] were examined. (A moderate [M] of 0.24 mm ([M]:[TA] = 1:1) was used to prepare these capsules.) The stability of the MPN capsules decreased as the pH decreased from 7.4 to 5.0 (Figure 3 a). At pH 5.0, over 25 % of the CuII-TA capsules (9.7 1.0 nm) disassembled within 1 h, whereas it took roughly 6 h for 25 % of the AlIIITA capsules (10.8 1.3 nm) to disassemble, and even after 168 h, less than 25 % of the ZrIV-TA capsules (14.2 1.5 nm) had disassembled. The intermediate disassembly kinetics for the AlIII-TA capsules correspond to a desirable profile for Figure 3. Controlled disassembly of MPN capsules. a) pH-dependent disassembly kinetics of CuII-TA, AlIII-TA and drug delivery, as the capZrIV-TA capsules at different pH values, as assessed by flow cytometry. The data are mean values standard sules are relatively stable deviation (SD; N = 3). b) Degradation of FITC-dextran-loaded AlIII-TA capsules in JAWS II cells at different times, at the pH of the blood- as imaged by deconvolution fluorescence microscopy. Green corresponds to FITC-dextran, red to the cell stream (7.4) and gradu- membrane staining, and blue to nuclear staining. The scale bars are 10 mm. 2014 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim
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. Angewandte Communications prepared by adding 5 MBq of 64Cu during MPN film assembly. Figure 4 b shows the corresponding PET phantom image, which suggests that the 64CuII-TA capsules are efficient PETactive vehicles, and useful for tracking the biodistribution of both loaded drugs and the carrier itself. Therefore, 64CuII-TA capsules were injected into healthy BALB/c mice. PET/ computed tomography (CT) scans were acquired and the biodistribution of the capsules was evaluated after 30 min. The PET/CT images showed major uptake of the capsules in the liver and minor uptake in the spleen (Figure 4 c), which was further confirmed by the postmortem biodistribution data (Figure S12). This gamma-counter data set revealed general tissue distribution and demonstrated that the 64CuII-TA capsules mainly accumulated in the liver and spleen, as a consequence of the reticuloendothelial system that processes microparticles.[7i] It is plausible that the biodistribution of 64CuII-TA capsules can be tailored by controlling capsule properties (e.g., size, shape, and surface chemistry) given the versatility of MPN materials.[10b] We then explored the possibility of generating MRI contrast agents by Figure 4. Engineering multifunctional MPN capsules for imaging. a) Normalized fluorescence spectra of the coordination of FeIII, capsule suspensions of EuIII-TTA-TA and TbIII-AA-TA excited at 360 nm. Insets are photographs of the MnII, and GdIII into MPN corresponding capsule suspensions (top), excited at 254 and 365 nm, and of PDMS coated with EuIII-TTA-TA capsules. We performed (bottom) excited at 365 nm. Scale bars are 1 cm. b) Pseudo-color PET phantom of suspensions of 64CuII-TA MR relaxometry experi8 capsules at different dilution ratios (stock suspension concentration is 3.2 10 capsules per millilitre with an 64 II ments with these capsules activity of 1 MBq). c) Small-animal PET/CT image of an in vivo model 30 min after injection of 1 MBq Cu -TA and determined their relaxcapsules (maximum intensity projection (right), sagittal view (left)). The color scale for all PET image data shows radiotracer uptake with white corresponding to the highest activity and blue to the lowest activity. ivities on a 9.4 T animal d) MRI phantom images of capsules immobilized in agarose. Shown are T1-weighted inversion recovery images MRI system (Figure 4 d,e (with inversion time TI = 1.375 ms) and T2-weighted spin echo images (with echo time TE = 50 ms) of samples and Figure S13). Among with three different metal concentrations from left to right: 0.02, 0.1, and 0.3 mm (0.15 mm for GdIII-TA). all three samples the MnIIIII II III e) Table of MRI relaxivities for Fe -TA, Mn -TA, and Gd -TA capsule suspensions measured with a 9.4 T animal TA capsules displayed the MRI system. highest relaxivity r2, which is of the order of 60 s1 mm 1 and generally sufficient for in vivo use.[21] fluorescence of the TbIII-AA-TA capsules is ascribed to the 5 D4 !7F5 transition around 545 nm.[20] The fluorescence We additionally examined the hybrid, dual-metal capsules intensity of the EuIII-TTA-TA capsules is dependent on the for improved functionality as biomedical imaging agents. To test dual-metal incorporation, we assembled (CuII/EuIII[EuIII], with an increase in fluorescence intensity dependent III on the [Eu ] (Figure S11). The insets of Figure 4 a show TTA)-TA capsules that displayed highly distributed signals from Cu and Eu by EDX mapping analysis (Figure 5 a). To photographs of the TbIII-AA-TA and EuIII-TTA-TA capsule verify the multimodal capability of MPN capsules, (64CuII/ suspensions (upper) and polydimethylsiloxane (PDMS) III coated with a Eu -TTA-TA film excited at 365 nm (lower). EuIII-TTA)-TA capsules were used for both PET and fluoWe extended the investigation of MPN capsules for rescence imaging. Figure 5 b shows the fluorescence and biomedical imaging by incorporating metals useful for reconstructed PET/CT images of an aqueous suspension of positron emission tomography (PET) and magnetic reso(64CuII/EuIII-TTA)-TA capsules. Furthermore, multicolor flu64 II nance imaging (MRI). Radioactive Cu -TA capsules were orescent MPN capsules were achieved by incorporating EuIII
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To impart imaging properties to the MPN capsules, we employed 2-thenoyltrifluoroacetone (TTA) and acetylacetone (AA) as coligands to enhance the fluorescence intensities of EuIII-TA and TbIII-TA capsules, respectively, and to demonstrate that guest functional ligands can be easily incorporated into MPN films. Figure 4 a shows the fluorescence spectra of these capsules. The red fluorescence observed in the EuIII-TTA-TA capsules is mainly attributed to the 5D0 !7F2 transition around 613 nm[19] and the green
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activity can be observed in RhIII-TA capsules when the reaction temperature changes from 50 to 70 8C; 16 to 103 mol mol1 h1, respectively. The catalytic activity of RhIII-TA capsules was significantly greater than RhCl(CO)(TPPTS)2 between 50 and 70 8C, where the maximum initial TOF of RhCl(CO)(TPPTS)2 was only 44 mol mol1 h1, which is 43 % of the TOF value for the RhIII-TA capsules. In summary, we introduced a library of MPNs for the engineering of multifunctional capsules. Various metals were coorFigure 5. Hybrid dual metal MPN capsules for multimodal imaging, multicolor properties, and tunable disassembly. dinated with tannic II III a) EDX elemental mapping of dual metal (Cu /Eu -TTA)-TA capsules. The scale bar is 1 mm. b) Fluorescence (left) acid to form thin films and PET/CT pseudo-color (right) images of a suspension of (64CuII/EuIII-TTA)-TA capsules. The scale bars are 1 cm. III III c) Normalized fluorescence spectra for (Eu -TTA/Tb -AA)-TA capsule suspensions excited at 312 nm. The insets are on particulate substrates. EDX mapping fluorescence images of EuIII-TTA-TA, TbIII-AA-TA, and (EuIII-TTA/TbIII-AA)-TA capsule suspensions and the corresponding locations on the CIE 1931 chromaticity diagram. d) pH-dependent disassembly kinetics of CuII-TA, ZrIV-TA analysis demonstrated and hybrid CuII/ZrIV-TA capsules at different pH, as assessed by flow cytometry. The data are mean values SD that the metals were (N = 3). incorporated for both single- and dual-metal MPN capsules. The disassembly of MPN capsules was controlled by changing and TbIII simultaneously (Figure 5 c). The strong yellow the metal species and feed concentrations. Similarly, varying fluorescence of the (EuIII-TTA/TbIII-AA)-TA capsules correthe feed concentration of the lanthanide metals allowed for sponds to the expected color in the CIE 1931 chromaticity control over the fluorescence intensity of the capsules. diagram (inset of Figure 5 c). The multicolor fluorescent Biomedical functionalities for drug delivery, PET, and MRI properties of the MPN films might be of interest in flexible were successfully imparted to the MPN capsules. The PET full-color displays, next-generation lighting sources, and activity allowed assessment of the biodistribution of MPN bioimaging agents necessary for deciphering multiple biologcapsules in vivo. The transverse relaxivity r2 of MnII-TA ical events simultaneously.[22] Additionally, the degradation profile of the MPN capsules could be tuned by incorporating capsules is, in principle, large enough for in vivo use of the two metals with different degradation kinetics (Figure 5 d). capsules as MRI contrast agents. Finally, it was demonstrated By varying the ratio of CuII :ZrIV, the kinetics of disassembly at that RhIII-TA capsules had improved catalysis properties different pH values can be tuned between the disassembly compared with a commercial catalyst. The ability to simultaprofiles of the single metal MPN capsules. neously incorporate multiple metals should facilitate the The wide variety of metals used to demonstrate MPN development of MPN capsules useful for a range of applicacapsule formation is not only limited to metals useful for tions. biomedical application. Therefore, we demonstrated the Received: December 23, 2013 catalytic function of RhIII-TA capsules for the hydrogenation Published online: && &&, &&&& of quinoline versus a commercial catalyst, RhCl(CO)(TPPTS)2 (TPPTS = triphenylphosphine-trisulfonated).[23] The initial hydrogenation activities (turnover of frequency, TOF) of both RhIII-TA capsules and RhCl(CO)(TPPTS)2 are Keywords: coordination · fluorescence · quite low when the reaction temperature is below 50 8C multifunctional capsules · organic–inorganic hybrid materials · (Figure S14). However, a dramatic increase in hydrogenation polyphenols
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Communications Organic–Inorganic Hybrid Materials J. Guo, Y. Ping, H. Ejima, K. Alt, M. Meissner, J. J. Richardson, Y. Yan, K. Peter, D. v. . Elverfeldt, C. E. Hagemeyer, F. Caruso* &&&&—&&&&
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Multifunctional capsules: A common plant phenolic compound, tannic acid, can be used to coordinate a variety of metals through a one-step assembly process, thereby yielding a broad library
of metal–phenolic network (MPN; see picture) capsules. The properties of the MPN capsules are determined by the coordinated metals.
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Engineering Multifunctional Capsules through the Assembly of Metal–Phenolic Networks
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Chemie
DOI: 10.1002/anie.201311136
Organic–Inorganic Hybrid Materials Hot Paper
Engineering Multifunctional Capsules through the Assembly of Metal– Phenolic Networks** Junling Guo, Yuan Ping, Hirotaka Ejima, Karen Alt, Mirko Meissner, Joseph J. Richardson, Yan Yan, Karlheinz Peter, Dominik v. Elverfeldt, Christoph E. Hagemeyer, and Frank Caruso* Abstract: Metal–organic coordination materials are of widespread interest because of the coupled benefits of inorganic and organic building blocks. These materials can be assembled into hollow capsules with a range of properties, which include selective permeability, enhanced mechanical/thermal stability, and stimuli-responsiveness. Previous studies have primarily focused on the assembly aspects of metal-coordination capsules; however, the engineering of metal-specific functionality for capsule design has not been explored. A library of functional metal–phenolic network (MPN) capsules prepared from a phenolic ligand (tannic acid) and a range of metals is reported. The properties of the MPN capsules are determined by the coordinated metals, allowing for control over film thickness, disassembly characteristics, and fluorescence behavior. Furthermore, the functional properties of the MPN capsules were tailored for drug delivery, positron emission tomography (PET), magnetic resonance imaging (MRI), and catalysis. The ability to incorporate multiple metals into MPN capsules demonstrates that a diverse range of functional materials can be generated.
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aturally occurring building blocks that can assemble into functional materials have long been a source for scientific inspiration.[1] A salient feature of natural materials is the exploitation of organic and inorganic building blocks to prepare hybrid materials with synergistic properties to meet complex biological requirements.[1a,d] For example, by using mild conditions to generate highly functional macroscopic inorganic–organic hybrids, crustaceans produce armoured carapaces,[1d] mollusks build ornate shells,[2] and vertebrates grow lightweight bones.[1d] Specifically, the coordination of
[*] J. Guo, Dr. Y. Ping, Dr. H. Ejima, J. J. Richardson, Dr. Y. Yan, Prof. F. Caruso Department of Chemical and Biomolecular Engineering The University of Melbourne, Parkville Victoria 3010 (Australia) E-mail: [email protected] Dr. K. Alt, Prof. K. Peter, Assoc. Prof. C. E. Hagemeyer Atherothrombosis and Vascular Biology/Vascular Biotechnology Baker IDI Heart and Diabetes Institute Melbourne, Victoria 3010 (Australia) M. Meissner, Prof. D. v. . Elverfeldt Department of Radiology, Medical Physics University Medical Center Freiburg Breisacher Str. 60a, Freiburg (Germany) [**] The authors acknowledge support of this research by the Australian Research Council under the Australian Laureate Fellowship FL120100030 (F.C.), Discovery Project DP0877360 (F.C.), Discovery Early Career Researcher Award DE130100488 (Y.Y.), and Future
Fellowship FT0992210 (K.P.) schemes. This work was supported by a project grant from the National Health and Medical Research Council (grant number 1029249; K.P. and C.E.H.). K.A. is supported by the German Research Foundation (grant number Al 1521/1-1). C.E.H. is supported by a National Heart Foundation Career Development Fellowship (grant number CR 11M 6066). The work was also supported in part by the Victorian Government’s Operational Infrastructure Support Program, Monash Biomedical Imaging and Victoria’s Science Agenda Strategic Project Fund. We acknowledge the Centre for PET at the Austin (Melbourne, Australia) for supply of the 64Cu. We thank X. Wang (Sichuan University) for assistance with the catalytic experiments, X. Duan (The University of Melbourne) for assistance with XPS analysis, Dr. K. Liang (The University of Melbourne) for assistance with deconvolution microscopy, and Dr. Ming Hu, Dr. Jiwei Cui, Yi Ju, and Tomoya Suma (The University of Melbourne) for helpful discussions. Supporting information for this article is available on the WWW under http://dx.doi.org/10.1002/anie.201311136.
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organic ligands with specific metal species plays a critical role in a range of biological functions,[3] such as photosynthesis (through MgII-porphyrin),[4] oxygen transportation (through CuII-heme)[5] and adhesion (through FeIII-phenolics).[6] Inspired by these natural examples, metal–organic coordination materials have attracted considerable interest in chemistry and materials science.[7] The assembly of metal–organic coordination materials into hollow capsules has recently attracted interest because of their desirable properties,[8] such as selective permeability,[9] high mechanical[10] and thermal[11] stability, and pH-responsive disassembly.[10b] Several assembly techniques, including liquid–liquid interfacial growth,[9a] spray-drying,[9b] and sacrificial template-mediated formation,[10–12] have been used to fabricate capsules based on metal-coordination interactions. However, these previous studies have not focused on the specific incorporation of a range of metals into the capsule shells, nor have the incorporated metals specifically been used to impart functionality into the capsules. The ability to incorporate diverse metals into metal–organic coordination capsules provides new opportunities for engineering multifunctional systems for various applications. Here, we demonstrate that a single organic ligand can coordinate with a variety of metals, and thereby provide a broad library of functional metal–phenolic networks (MPNs). Because of the diverse chelation ability of phenolic materials,[13] tannic acid (TA; see Figure S1 in the Supporting Information), a ubiquitous natural polyphenol, is coordinated to 18 different metal ions (M), including aluminium (Al), vanadium (V), chromium (Cr), manganese (Mn), iron (Fe), cobalt (Co), nickel (Ni), copper (Cu), zinc (Zn), zirconium
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. Angewandte Communications Furthermore, the XPS survey scan spectra confirmed the presence of metal in the capsule shells (Figure S4). TA showed a major peak at 533.5 eV and a relatively small peak at 529.4 eV, which can be ascribed to the C=O and HOC groups, respectively.[14] After chelation with metal ions, the peak of the HOC group in the O1s spectra shifted from 529.4 eV to a higher binding energy of 531.8 eV (Figure S5, CuII-TA capsules), which suggests electron transfer from TA to the metals.[15] The MPN films (CuII-TA) are amorphous materials, as confirmed by X-ray diffraction data (Figure S6).[16] The morphology of the capsules was characterized by differential interference contrast (DIC) microscopy, scanning electron microscopy (SEM), transmission electron microscopy (TEM), and atomic force microscopy (AFM) (Figure 2, Figures S7 and S8). The MPN capsules were monodisperse and spherical, as observed by DIC microscopy and freezedried SEM (Figure 2 a, inset). SEM, TEM, and AFM showed collapsed capsules, with folds and creases similar to air-dried polymeric hollow capsules.[17] No excess coordination cluster aggregates were observed on the surface of the MPN capsules in TEM (Figure 2 b) or AFM (Figure 2 c). Energy-dispersive X-ray (EDX) mapping analysis of MPN capsules Figure 1. Assembly of MPN capsules from various metals. a) Assembly of TA and metal ions to form a MPN demonstrated that the metal film on a particulate template, followed by the subsequent formation of a MPN capsule. b) Periodic table: distribution patterns metals highlighted in orange are used to form MPN capsules in this study. Metals highlighted in green show other metals that may be used for MPN capsule preparation based on previous studies on metal-coordination matched well with highwith phenolics in bulk solution. c) DIC images of MPN capsules prepared from different metals. Scale bars angle annular dark-field are 5 mm. Inset images are photographs of MPN capsule suspensions. images (HAADF) and the distribution patterns of C and O maps (Figure 2 d). This confirms that the metals were associated with TA and MPN films were formed simply by mixing TA and metal well distributed in the MPN films. AFM was used to probe the solutions in the presence of a substrate (Figure 1 a). When material differences between MPN capsules prepared from using particulate templates, highly monodisperse capsules metals of different oxidation numbers: CuII-TA, AlIII-TA, and containing a broad range of metals were obtained after template removal (Figure 1 c). The coordination between TA ZrIV-TA (Figure S9). The thickness and stability of the MPN and metals was confirmed by UV/Vis absorption spectrophofilms are dependent on the choice of metal and the metal feed tometry, Fourier transform infrared spectrophotometry (FTconcentration (hereafter denoted [M]). Notably, comparison IR) and X-ray photoelectron spectroscopy (XPS). UV/Vis of film thicknesses among these three MPN capsules showed spectra of MPN capsule suspensions show new absorbance that ZrIV-TA capsules were the thickest and CuII-TA capsules peaks after metal chelation, which suggests coordination the thinnest. The film thickness of CuII-TA capsules increased between TA and the respective metals (Figure S2). FT-IR from 9.0 0.8 nm to 10.7 1.5 nm when the feed [CuII] III spectra of the Fe -TA MPN capsules (air-dried) also indicate changed from 0.08 ([CuII]:[TA] = 1:3) to 0.72 mm that the phenolic groups coordinated with metal ions, as ([CuII]:[TA] = 3:1). Similarly, the minimum thickness of evidenced by the reduced intensity of the HOC stretching ZrIV-TA capsules was 11.9 1.2 nm ([ZrIV]:[TA] = 1:3), and peak when compared with non-coordinated TA (Figure S3). raising the [ZrIV] increased the film thickness to 15.4 2.2 nm
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(Zr), molybdenum (Mo), ruthenium (Ru), rhodium (Rh), cadmium (Cd), cerium (Ce), europium (Eu), gadolinium (Gd), and terbium (Tb), to generate robust MPN films capable of forming hollow structured capsules (Figure 1). Given the facile preparation process, and the capacity to incorporate single and multiple metals, MPN capsules are a promising class of multifunctional materials. These MPN capsules are herein characterized and used for diverse applications, including drug delivery, biomedical imaging, and catalysis.
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ally disassemble at lower pH values that correspond to those in endosomal and lysosomal compartments (5.0– 6.0). The cytotoxicity of the AlIII-TA capsules was determined to be negligible (Figure S10), hence the drug delivery properties of the AlIII-TA capsules were investigated with model cargo (dextranfluorescein isothiocyanate, FITC-dextran). These capsules were incubated with JAWS II cells for different times. The cellular membranes were stained with AlexaFluor (AF) 594-wheat germ agglutinin, and internalization of Figure 2. Structural characterization of MPN capsules. a) SEM, b) TEM, and c) AFM images of CuII-TA these capsules was verified by capsules. d) EDX elemental mapping of CuII-TA, AlIII-TA and ZrIV-TA capsules. Scale bars are 2 mm in (a–c), deconvolution fluorescence 2 mm in the inset of (a), 200 nm in the inset of (b) and 1 mm in (d). microscopy (Figure 3 b). At the time interval of 16 h, most internalized AlIII-TA IV III capsules were intact, retaining their original spherical shape ([Zr ]:[TA] = 3:1). The film thicknesses of Al -TA films, (see yellow arrows in Figure 3 b). With increasing incubation which increased from 9.9 1.3 nm to 13.6 1.3 nm, showed time (to 24 h), a larger number of deformed and disassembled a similar trend to CuII-TA and ZrIV-TA. We note that below AlIII-TA capsules were observed (see white arrows in Figa [M] of 0.08 mm, capsules for all three metals were difficult to form, while above 0.72 mm the capsules aggregated. ure 3 b). The intracellular disassembly of AlIII-TA capsules The pH-disassembly kinetics of the MPN capsules preprovides the potential for tailored drug release, which is of pared from each of the three model metals (CuII, AlIII, ZrIV) importance for advanced drug delivery.[18] were examined. (A moderate [M] of 0.24 mm ([M]:[TA] = 1:1) was used to prepare these capsules.) The stability of the MPN capsules decreased as the pH decreased from 7.4 to 5.0 (Figure 3 a). At pH 5.0, over 25 % of the CuII-TA capsules (9.7 1.0 nm) disassembled within 1 h, whereas it took roughly 6 h for 25 % of the AlIIITA capsules (10.8 1.3 nm) to disassemble, and even after 168 h, less than 25 % of the ZrIV-TA capsules (14.2 1.5 nm) had disassembled. The intermediate disassembly kinetics for the AlIII-TA capsules correspond to a desirable profile for Figure 3. Controlled disassembly of MPN capsules. a) pH-dependent disassembly kinetics of CuII-TA, AlIII-TA and drug delivery, as the capZrIV-TA capsules at different pH values, as assessed by flow cytometry. The data are mean values standard sules are relatively stable deviation (SD; N = 3). b) Degradation of FITC-dextran-loaded AlIII-TA capsules in JAWS II cells at different times, at the pH of the blood- as imaged by deconvolution fluorescence microscopy. Green corresponds to FITC-dextran, red to the cell stream (7.4) and gradu- membrane staining, and blue to nuclear staining. The scale bars are 10 mm. 2014 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim
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. Angewandte Communications prepared by adding 5 MBq of 64Cu during MPN film assembly. Figure 4 b shows the corresponding PET phantom image, which suggests that the 64CuII-TA capsules are efficient PETactive vehicles, and useful for tracking the biodistribution of both loaded drugs and the carrier itself. Therefore, 64CuII-TA capsules were injected into healthy BALB/c mice. PET/ computed tomography (CT) scans were acquired and the biodistribution of the capsules was evaluated after 30 min. The PET/CT images showed major uptake of the capsules in the liver and minor uptake in the spleen (Figure 4 c), which was further confirmed by the postmortem biodistribution data (Figure S12). This gamma-counter data set revealed general tissue distribution and demonstrated that the 64CuII-TA capsules mainly accumulated in the liver and spleen, as a consequence of the reticuloendothelial system that processes microparticles.[7i] It is plausible that the biodistribution of 64CuII-TA capsules can be tailored by controlling capsule properties (e.g., size, shape, and surface chemistry) given the versatility of MPN materials.[10b] We then explored the possibility of generating MRI contrast agents by Figure 4. Engineering multifunctional MPN capsules for imaging. a) Normalized fluorescence spectra of the coordination of FeIII, capsule suspensions of EuIII-TTA-TA and TbIII-AA-TA excited at 360 nm. Insets are photographs of the MnII, and GdIII into MPN corresponding capsule suspensions (top), excited at 254 and 365 nm, and of PDMS coated with EuIII-TTA-TA capsules. We performed (bottom) excited at 365 nm. Scale bars are 1 cm. b) Pseudo-color PET phantom of suspensions of 64CuII-TA MR relaxometry experi8 capsules at different dilution ratios (stock suspension concentration is 3.2 10 capsules per millilitre with an 64 II ments with these capsules activity of 1 MBq). c) Small-animal PET/CT image of an in vivo model 30 min after injection of 1 MBq Cu -TA and determined their relaxcapsules (maximum intensity projection (right), sagittal view (left)). The color scale for all PET image data shows radiotracer uptake with white corresponding to the highest activity and blue to the lowest activity. ivities on a 9.4 T animal d) MRI phantom images of capsules immobilized in agarose. Shown are T1-weighted inversion recovery images MRI system (Figure 4 d,e (with inversion time TI = 1.375 ms) and T2-weighted spin echo images (with echo time TE = 50 ms) of samples and Figure S13). Among with three different metal concentrations from left to right: 0.02, 0.1, and 0.3 mm (0.15 mm for GdIII-TA). all three samples the MnIIIII II III e) Table of MRI relaxivities for Fe -TA, Mn -TA, and Gd -TA capsule suspensions measured with a 9.4 T animal TA capsules displayed the MRI system. highest relaxivity r2, which is of the order of 60 s1 mm 1 and generally sufficient for in vivo use.[21] fluorescence of the TbIII-AA-TA capsules is ascribed to the 5 D4 !7F5 transition around 545 nm.[20] The fluorescence We additionally examined the hybrid, dual-metal capsules intensity of the EuIII-TTA-TA capsules is dependent on the for improved functionality as biomedical imaging agents. To test dual-metal incorporation, we assembled (CuII/EuIII[EuIII], with an increase in fluorescence intensity dependent III on the [Eu ] (Figure S11). The insets of Figure 4 a show TTA)-TA capsules that displayed highly distributed signals from Cu and Eu by EDX mapping analysis (Figure 5 a). To photographs of the TbIII-AA-TA and EuIII-TTA-TA capsule verify the multimodal capability of MPN capsules, (64CuII/ suspensions (upper) and polydimethylsiloxane (PDMS) III coated with a Eu -TTA-TA film excited at 365 nm (lower). EuIII-TTA)-TA capsules were used for both PET and fluoWe extended the investigation of MPN capsules for rescence imaging. Figure 5 b shows the fluorescence and biomedical imaging by incorporating metals useful for reconstructed PET/CT images of an aqueous suspension of positron emission tomography (PET) and magnetic reso(64CuII/EuIII-TTA)-TA capsules. Furthermore, multicolor flu64 II nance imaging (MRI). Radioactive Cu -TA capsules were orescent MPN capsules were achieved by incorporating EuIII
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To impart imaging properties to the MPN capsules, we employed 2-thenoyltrifluoroacetone (TTA) and acetylacetone (AA) as coligands to enhance the fluorescence intensities of EuIII-TA and TbIII-TA capsules, respectively, and to demonstrate that guest functional ligands can be easily incorporated into MPN films. Figure 4 a shows the fluorescence spectra of these capsules. The red fluorescence observed in the EuIII-TTA-TA capsules is mainly attributed to the 5D0 !7F2 transition around 613 nm[19] and the green
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activity can be observed in RhIII-TA capsules when the reaction temperature changes from 50 to 70 8C; 16 to 103 mol mol1 h1, respectively. The catalytic activity of RhIII-TA capsules was significantly greater than RhCl(CO)(TPPTS)2 between 50 and 70 8C, where the maximum initial TOF of RhCl(CO)(TPPTS)2 was only 44 mol mol1 h1, which is 43 % of the TOF value for the RhIII-TA capsules. In summary, we introduced a library of MPNs for the engineering of multifunctional capsules. Various metals were coorFigure 5. Hybrid dual metal MPN capsules for multimodal imaging, multicolor properties, and tunable disassembly. dinated with tannic II III a) EDX elemental mapping of dual metal (Cu /Eu -TTA)-TA capsules. The scale bar is 1 mm. b) Fluorescence (left) acid to form thin films and PET/CT pseudo-color (right) images of a suspension of (64CuII/EuIII-TTA)-TA capsules. The scale bars are 1 cm. III III c) Normalized fluorescence spectra for (Eu -TTA/Tb -AA)-TA capsule suspensions excited at 312 nm. The insets are on particulate substrates. EDX mapping fluorescence images of EuIII-TTA-TA, TbIII-AA-TA, and (EuIII-TTA/TbIII-AA)-TA capsule suspensions and the corresponding locations on the CIE 1931 chromaticity diagram. d) pH-dependent disassembly kinetics of CuII-TA, ZrIV-TA analysis demonstrated and hybrid CuII/ZrIV-TA capsules at different pH, as assessed by flow cytometry. The data are mean values SD that the metals were (N = 3). incorporated for both single- and dual-metal MPN capsules. The disassembly of MPN capsules was controlled by changing and TbIII simultaneously (Figure 5 c). The strong yellow the metal species and feed concentrations. Similarly, varying fluorescence of the (EuIII-TTA/TbIII-AA)-TA capsules correthe feed concentration of the lanthanide metals allowed for sponds to the expected color in the CIE 1931 chromaticity control over the fluorescence intensity of the capsules. diagram (inset of Figure 5 c). The multicolor fluorescent Biomedical functionalities for drug delivery, PET, and MRI properties of the MPN films might be of interest in flexible were successfully imparted to the MPN capsules. The PET full-color displays, next-generation lighting sources, and activity allowed assessment of the biodistribution of MPN bioimaging agents necessary for deciphering multiple biologcapsules in vivo. The transverse relaxivity r2 of MnII-TA ical events simultaneously.[22] Additionally, the degradation profile of the MPN capsules could be tuned by incorporating capsules is, in principle, large enough for in vivo use of the two metals with different degradation kinetics (Figure 5 d). capsules as MRI contrast agents. Finally, it was demonstrated By varying the ratio of CuII :ZrIV, the kinetics of disassembly at that RhIII-TA capsules had improved catalysis properties different pH values can be tuned between the disassembly compared with a commercial catalyst. The ability to simultaprofiles of the single metal MPN capsules. neously incorporate multiple metals should facilitate the The wide variety of metals used to demonstrate MPN development of MPN capsules useful for a range of applicacapsule formation is not only limited to metals useful for tions. biomedical application. Therefore, we demonstrated the Received: December 23, 2013 catalytic function of RhIII-TA capsules for the hydrogenation Published online: && &&, &&&& of quinoline versus a commercial catalyst, RhCl(CO)(TPPTS)2 (TPPTS = triphenylphosphine-trisulfonated).[23] The initial hydrogenation activities (turnover of frequency, TOF) of both RhIII-TA capsules and RhCl(CO)(TPPTS)2 are Keywords: coordination · fluorescence · quite low when the reaction temperature is below 50 8C multifunctional capsules · organic–inorganic hybrid materials · (Figure S14). However, a dramatic increase in hydrogenation polyphenols
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Communications Organic–Inorganic Hybrid Materials J. Guo, Y. Ping, H. Ejima, K. Alt, M. Meissner, J. J. Richardson, Y. Yan, K. Peter, D. v. . Elverfeldt, C. E. Hagemeyer, F. Caruso* &&&&—&&&&
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Multifunctional capsules: A common plant phenolic compound, tannic acid, can be used to coordinate a variety of metals through a one-step assembly process, thereby yielding a broad library
of metal–phenolic network (MPN; see picture) capsules. The properties of the MPN capsules are determined by the coordinated metals.
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Engineering Multifunctional Capsules through the Assembly of Metal–Phenolic Networks
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